Metabolic Effects of Bariatric Surgery

R Corcelles and others Bariatric surgery 174:1 R19–R28 Review

MANAGEMENT OF ENDOCRINE DISEASE Metabolic effects of bariatric surgery

Ricard Corcelles1,2, Christopher R Daigle1 and Philip R Schauer1 Correspondence should be addressed 1Bariatric and Metabolic Institute, Cleveland Clinic, 9500 Euclid Avenue, M61 Cleveland, OH 44195, USA and to P R Schauer 2Department of Gastrointestinal Surgery, Institute of Digestive and Metabolic Diseases, Fundacio´ Clı´nic per a la Email Recerca Biome` dica, Hospital Clinic de Barcelona, Barcelona, Spain [email protected]

Abstract

Obesity is associated with an increased risk of type 2 diabetes, hypertension, dyslipidemia, cardiovascular disease, osteoarthritis, numerous cancers and increased mortality. It is estimated that at least 2.8 million adults die each year due to obesity-related cardiovascular disease. Increasing in parallel with the global obesity problem is metabolic syndrome, which has also reached epidemic levels. Numerous studies have demonstrated that bariatric surgery is associated with signiﬁcant and durable weight loss with associated improvement of obesity-related comorbidities. This review aims to summarize the effects of bariatric surgery on the components of metabolic syndrome (hyperglycemia, hyperlipidemia and hypertension), weight loss, perioperative morbidity and mortality, and the long-term impact on cardiovascular risk and mortality.

European Journal of Endocrinology (2016) 174, R19–R28

Introduction

Obesity is an epidemic on the rise. The World Health also reached epidemic levels. The National Health and

European Journal of Endocrinology Organization projects that by 2015, w2.3 billion adults Nutrition Examination Survey reported that 34% of will be overweight and more than 700 million will be American adults have metabolic syndrome based on the obese (1). Obesity is associated with an increased risk of National Cholesterol Education Program Adult Treatment type 2 diabetes (T2DM), hypertension, dyslipidemia, Panel III criteria: waist circumference R102 cm (men) cardiovascular disease, osteoarthritis, numerous cancers or R88 cm (women), triglycerides R150 mg/dl, HDL and increased mortality (2). It is estimated that at least 2.8 !40 mg/dl (men) or !50 mg/dl (women), hypertension million adults die each year due to obesity-related R130/85 mmHg and fasting glucose R100 mg/dl (4). cardiovascular disease (3). Increasing in parallel with the Conventional treatments such as diet, lifestyle modiﬁ- global obesity problem is metabolic syndrome, which has cation, exercise and pharmacotherapy have failed to

Invited Authors’ profiles Ricard Corcelles is consultant surgeon, Division of Gastrointestinal Surgery, Hospital Clıńic Barcelona, University of Barcelona, Spain. He specializes in the field of minimally invasive surgery and has dedicated part of his career to the realm of metabolic and bariatric surgery.

Philip R Schauer is Chief of Minimally Invasive General Surgery and Director of the Cleveland Clinic Bariatric and Metabolic Institute. He is also Professor of Surgery at the Cleveland Clinic Lerner College of Medicine of Case Western Reserve University. In addition, he is a former president of the American Society for Metabolic and Bariatric Surgery.

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achieve satisfactory sustained weight loss. In addition, the approaches. A retrospective review of the Bariatric Out- direct cost of obesity in the United States is extremely comes Longitudinal Database (BOLD) from 2007 to 2010 high, with an estimated $190 billion spent in 2010 (5). showed 79% EWL for BPD-DS compared with 67% EWL for Numerous studies have demonstrated that bariatric RYGB at 2 years follow-up (18). surgery is associated with significant and durable weight While O’Brien et al. (19) have recently reported 47% loss and associated improvement of obesity-related EWL in a cohort of 3227 patients followed over a 15-year comorbidities (6, 7, 8). Furthermore, the beneficial effects span, AGB is still considered a purely restrictive procedure of bariatric surgery on mortality, overall disease-specific with the lowest durable weight loss. For instance, a recent risk reduction and long-term quality of life are well meta-analysis by Chakravarty et al. (20) including five documented (9, 10, 11, 12). The degree of the effect on randomized controlled trials comparing AGB with other obesity-related comorbid conditions depends on the procedures concluded that AGB is associated with less bariatric surgical approach, typically classified based on weight loss. Since its introduction in 2007, SG case its restrictive and/or malabsorptive effect. Current data volumes have increased dramatically, with published from the International Federation for the Surgery of weight loss results comparable to RYGB. SG is considered Obesity and Metabolic Diseases (IFSO) reports that the a restrictive procedure; however, it has been increasingly most commonly performed procedures are the Roux-en-Y recognized to have metabolic effects similar to those gastric bypass (RYGB) (45%), sleeve gastrectomy (SG) observed after RYGB (21). A recent 5-year outcomes study (37%), adjustable gastric banding (AGB) (10%) and has reported successful SG results, with an 86% average biliopancreatic diversion (BPD) with or without duodenal EWL (22). However, other studies have demonstrated switch (DS) (2.5%) (13). This review aims to summarize the more modest long-term weight loss results (especially in effects of bariatric surgery on the components of metabolic patients with BMI O50 kg/m2), with many patients syndrome (hyperglycemia, hyperlipidemia and hyperten- ultimately requiring revision surgery for inadequate sion), weight loss, perioperative morbidity and mortality, weight loss or recidivism (23). and the long-term impact on cardiovascular risk and mortality. Complications of metabolic surgery

In their systematic review and meta-analysis (the most Weight loss cited paper in bariatric surgery), Buchwald et al. (24) Historically, the primary endpoint of bariatric surgical reported exceptionally low early and late mortality rates

European Journal of Endocrinology procedures has been weight loss and the reported weight after bariatric operations (0.28 and 0.35% respectively). loss achieved is generally sustained (14, 15). The overall Mortality was higher in open and conversion cases (0.30 percentage of excess weight loss (EWL) has been reported and 0.07% respectively), the male gender (male:female to be 47–70% in long-term series (16). Unfortunately, ratio of 4.7:01) and super obese subjects (range, 0.8–1.2%). there is a relative lack of randomized controlled trials with Open cases were considered those undergoing bariatric long-term results addressing this primary endpoint. In the surgery via laparotomy, while conversions were defined as controlled Swedish Obesity Study (SOS), patients were conversion from a laparoscopic procedure to an open prospectively followed over 20 years and those who (conventional) surgery (24). Similarly, a prospective, underwent bariatric surgery retained 18% of weight loss multicenter, observational study of 30-day outcomes in compared to 1% in the non-surgical group. The mean 4776 consecutive patients undergoing bariatric surgical 20-year weight reduction was 15% for AGB and 25% for procedures reported a comparably low perioperative RYGB patients (14). A systematic review conducted by mortality rate of 0.3% (8). O’Brien et al. (17) detected sustained EWL O50% for AGB After bariatric surgery, cardiopulmonary compli- and RYGB at 8 and 10 years respectively. cations such as myocardial infarction and pulmonary Malabsorptive procedures such as BPD and RYGB embolism are the major causes of mortality, representing achieve a greater percentage of EWL and more durable 70% of all deaths (25). The overall mortality rate for RYGB weight loss when compared to purely restrictive performed in centers of excellence is 0.4% (8). The most operations. However, this benefit comes at a cost of serious procedure-specific early complication after RYGB is higher complications rates. Specifically, BPD provides anastomotic leakage, with an incidence ranging from 0.1 the greatest weight loss in most published series but also to 5.6%. Patients at higher risk are those with higher BMI, has higher complication rates than less aggressive bariatric older age, males, with multiple comorbidities, smoking,

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or prior revision operations. AGB is a safe procedure with nutritional complications is mandatory following these 0.3% or less mortality rate (26). However, late compli- procedures (23). cations such as band slippage, erosion, migration, port infection and gastroesophageal perforations are well documented and occur in about 20% of patients (27). Metabolic outcomes of bariatric surgery In addition, long-term weight loss failure rates of over Effects on glycemic control 50% have been reported, and this has led to a significant increase in revisions of AGB to RYGB or SG (28). Substantial evidence from observational data indicates Procedure-specific late complications presenting clini- that bariatric surgery is very effective in controlling T2DM, cally as bowel obstruction after RYGB include internal with high remission rates and reductions in anti-diabetic hernias and gastrojejunal anastomotic stricture. Internal drug usage. Yet, not all bariatric procedures have hernias are more common after laparoscopic cases and demonstrated the same impact on glucose homeostasis. range from 0.5 to 9.0% (29). Abdominal pain with or In the first large meta-analysis (nZ22 094) published in without clinical signs of bowel obstruction is the most 2004, Buchwald et al. found that bariatric surgery achieved common presentation, and diagnostic laparoscopy is the complete diabetes resolution in 76.8% of subjects. The method of choice due to high false negative rates results differed dramatically by the type of surgery, associated with abdominal computerized tomography ranging from 48% remission rates with AGB to 84% (CT) scans (30). The incidence of gastrojejunal anastomo- remission rates with RYGB and 99% remission with tic stricture is about 10% and possible mechanisms biliopancreatic procedures (16). The authors concluded include ischemia, excessive scarring, recurrent marginal that malabsorptive procedures were the most effective ulcer and technical considerations such as excessive with respect to T2DM control. Data from the BOLD, a tension or torsion of the anastomosis. Endoscopy is the national database for the American Society for Metabolic preferred tool for both diagnosis and treatment of and Bariatric Surgery (ASMBS) Center of Excellence gastrojejunal stricture (31). Gastrointestinal bleeding Program (nZ23 106 patients), reported the highest after RYGB is another uncommon late complication, 12-month diabetes remission rates for BPD-DS (74%), typically caused by marginal ulceration. Marginal ulcers followed by RYGB (62%), SG (52%) and AGB (28%) (36). occur in 2% of patients within the first postoperative year, Many observational studies have reported long-term and then in 0.5% for up to 5 years (32). However, a recent diabetes remission rates (14, 37). A meta-analysis con- study has shown significantly higher marginal ulceration ducted by Buchwald et al. (38) including 621 studies with

European Journal of Endocrinology rates (34%) in 328 symptomatic patients who underwent 135 246 patients (all types of bariatric surgery) reported endoscopic exploration after RYGB. Uni- and multi-variate that 78% of diabetic patients had complete resolution analyses for associated risk factors identified tobacco as the (HbA1c !6.5% and no anti-diabetic drugs) and 86.6% had most significant risk factor for marginal ulceration diabetes improvement. Several factors have been reported recurrence (33). to be predictors of T2DM remission, including shorter Major nutritional complications are typically associ- duration of diabetes, greater weight loss, previous treat- ated with the malabsorptive effect of bariatric procedures ment with lifestyle modification and former oral anti- and are usually seen after BPD, RYGB and, less commonly, diabetic agent usage. Conversely, longer duration of AGB. Anemia is extremely common after RYGB and iron diabetes, decreased weight loss, severity of diabetes and deficiency ranges from 17 to 50%; the etiology is believed insulin requirements are factors associated with to be multifactorial in nature. Importantly, Love et al. (34) inadequate glycemic control after surgery (23, 39, 40). reported an iron deficiency incidence of up to 50% in In a study by Brethauer et al. (41) clinical outcomes of premenopausal women. Deficiencies in other trace 217 patients with T2DM who underwent bariatric surgery minerals (selenium, zinc and cooper) and vitamins (B12, between 2004 and 2007 and had at least 5-year follow-up B1, A, E, D and K) are commonly observed after bariatric were assessed (RYGB, nZ162; AGB, nZ32; SG, nZ23). procedures (35), specifically after BPD with or without DS Complete remission was defined as HbA1c !6% and (50–69%). Severe calcium and vitamin D deficiencies have fasting blood glucose !100 mg/dl off diabetic medi- been described after BPD and very long limb RYGB, cations. The mean EWL was 55% and the mean HbA1c leading to decreased bone mineral density and osteo- level decreased from 7.5G1.5% to 6.5G1.2% (P!0.001). porosis. Protein malnutrition can also occur after these Shorter duration of T2DM (P!0.001) and higher long- malabsorptive operations, and lifelong monitoring for term EWL (PZ0.006) predicted long-term remission.

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Recurrence of T2DM after initial remission occurred in RYGB cohort and least in the conventional medical 19% and was associated with longer duration of T2DM therapy group (45). The Diabetes Surgery Study was a (PZ0.03), less EWL (PZ0.02), and weight regain 12-month non-blinded randomized trial involving 120 (PZ0.015). Of note, the number of years after bariatric participants (T2DM for at least 6 months, HbA1c level of surgery is another predictive factor of relapse of diabetes 8.0% or higher and BMI 30–40 kg/m2) at four teaching that has been reported in the literature (40). hospitals in the United States and Taiwan (43). In this While many non-controlled studies have reported study, intensive lifestyle modification and medical inter- excellent improvements in glycemic control after vention was compared to RYGB. The primary endpoint bariatric surgery, direct comparisons with intense medical (HbA1c level below 7%) was reached by 48.5% of the RYGB treatment are scarce. The results of the SOS study, a cohort and 19% of the medical therapy group. However, non-randomized trial comparing medical therapy with patients in the surgical arm had 50% more serious bariatric surgery, demonstrated higher rates of diabetes adverse events than the medical treatment-only group. resolution at 2, 10 and 20 years follow-up in the bariatric Liang et al. compared three treatment arms in 108 obese surgery cohorts (14). The SOS study also reported T2DM patients with hypertension: conventional medical significant benefits in the surgical arms with regards to therapy, conventional medical therapy plus Exenatide long-term complications, major cardiovascular events and (glucagon-like peptide-1 agonist) and surgical interven- mortality of any cause. However, the SOS study investi- tion (RYGB). At 12 months follow-up, diabetes remission gators have recently reported a decline in T2DM remission had occurred in neither of the medical therapy groups rates at 15 years follow-up from 72.3 to 30.4% (42). vs 90% in the metabolic surgery arm. There was a Five short-term (1–2 years follow-up) randomized significant decrease in antihypertensive drug require- controlled trials comparing bariatric surgery with medical ments in the surgical group compared with medical treatment have been published (42, 43, 44, 45, 46, 47). The groups (P!0.05) (47). first randomized controlled trial by Dixon et al. in 2008 We recently published the STAMPEDE 3-year out- evaluated laparoscopic AGB vs pharmacotherapy and comes (randomization of 150 patients with uncontrolled lifestyle intervention (nZ60, obese patients with T2DM). T2DM to intensive medical therapy alone or intensive The surgical group achieved T2DM remission in 73% medical therapy plus RYGB or SG) with 91% of patients compared to 13% in the nonsurgical group (2 years follow- completing follow-up. At 36 months, the primary end- up). Of note, weight loss was significantly higher in the point (HbA1c level %6%) was achieved by 5% of patients surgical group (20.7% vs 1.7%) (42). Mingrone et al. in the medical group compared with 38% in the RYGB arm

European Journal of Endocrinology randomly assigned 60 obese T2DM patients to receive and 24% in the SG arm (PZ0.01) (46). Furthermore, the conventional medical therapy or undergo either RYGB or use of anti-diabetic medications (including insulin) was BPD. Subjects included in the trial had diabetes for at least lower in both surgical groups when compared to the 5 years, BMI R35 kg/m2, and HbA1c of 7.0% or greater. medial therapy cohort. The surgically treated patients had The major endpoint was the rate of remission (defined as improved glycemic control at 3 years and more than 90% HbA1c level !6.5%). At 2 years, the remission rate was 0% of patients had glycemic control without the use of for medical treatment, 75% for the RYGB group and 95% insulin. Weight loss and shorter duration of diabetes in the BPD group (P!0.001 for both comparisons) (44). were the main predictors of HbA1c level %6% after surgery At the Cleveland Clinic, we randomized 150 patients (46). The results of our study suggest that bariatric surgery with T2DM to conventional medical therapy, RYGB or SG. is superior to intensive medical therapy alone in glycemic The primary endpoint of the ‘Surgical Treatment and control after 3 years of randomization. Medications Potentially Eradicate Diabetes Efficiently’ (STAMPEDE) study was the proportion of patients achiev- Mechanisms underlying glycemic control ing HbA1c of 6.0% or less 12 months after treatment. A total of 42% in the RYGB arm, 37% in the SG arm and 12% There are many theories with regard to the mechanisms in the medical group achieved remission at 1 year. The underlying the beneficial metabolic effects of bariatric mean HbA1c level was 7.5G1.8% in the medical therapy surgery. Several studies have reported early resolution of group, 6.6G1.0% in the SG group, and 6.4G0.9% in the T2DM 1 month after RYGB, with metabolic improvements RYGB group. Mean weight loss was 5.4 kg in the medically greater than expected for the magnitude of weight lost (48). treated group vs 25.1 and 29.4 kg in the SG and RYGB These data suggest a weight loss-independent effect of groups, respectively. Complications were higher in the RYGB on glucose homeostasis control. Conversely,

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glycemic improvement following AGB appears to be The results of pharmacological blockade of the action of related to the amount of weight loss. Thus, AGB appears GLP-1 on its receptor (promoting prandial insulin release to lack weight-independent effects on metabolic disease inhibition) tend to argue against GLP-1 being critical in since remission of diabetes occurs gradually and in parallel diabetes remission after SG or RYGB. Several studies have with weight loss (42). shown modest impairment in glycemic control after The mechanisms by which RYGB improves metabolic GLP-1 receptor blockade, indicating that the contribution profiles have been thoroughly studied. In addition to the of endogenous GLP-1 after bariatric surgery to pancreatic restriction related to the gastric pouch and the malabsorp- beta cell function may only be minor (62). tion associated with bypassing the proximal small bowel, The SG operation (no gastrointestinal rearrange- there are two accepted theories on the benefits of RYGB on ments) has also been shown to have metabolic effects. T2DM control (49). The ‘foregut hypothesis’ is based on the Many studies have shown incretin upregulation after SG importance of duodenal exclusion and is supported by rat (63) and some reports suggest that RYGB and SG are studies where the duodenal-jejunal bypass leads to glycemic associated with comparable remission rates of T2DM (64). improvement. Interestingly, this beneficial effect is not Numerous other factors have been implicated as sustained when the gastro-jejunal nutrient transit is restored potential contributors in the metabolic improvement (50). Novel devices like the EndoBarrier Endoluminal Sleeve observed after bariatric surgery including other intestinal (GI Dynamics Inc., Lexington, MA, USA) try to mimic the gut hormones (GLP-2, PYY), ghrelin (anorexic hormone anti-diabetic effect of RYGB by excluding the duodenum secreted by the gastric fundus), adipokines, the increased and proximal jejunum from nutrient transit (based on the energy expenditure following surgery, changes in the gut ‘foregut hypothesis’) (51). In contrast, the ‘hindgut microbiome and bile acid (BA) metabolism (49). hypothesis’ is supported by the observation that rapid BA are increasingly recognized as molecules with delivery of nutrients to the distal small bowel results in endocrine functions, and a link between BA and exaggerated gut hormone secretion, in particular GLP-1. glycemic control has been suggested. Human studies and This hypothesis is best illustrated in animal studies where animal models support that RYGB promotes a rise in rats undergo ileal interposition surgery (interposition of a BA concentrations (65). Plasma BA bind to the G-protein- segment of ileum to a segment of proximal small bowel) that coupled receptor (TGR5) that is present in enteroendocrine has shown similar effects to those observed via RYGB (52). cells, liver, skeletal muscle and brown adipose tissue. The GLP-1 has numerous metabolic effects but probably activation of TGR5 increases GLP-1 release, which can the most important is its ability to enhance B-cell function improve insulin secretion and insulin sensitivity (66).

European Journal of Endocrinology (53). The rapid entry and absorption of nutrients in the BA are also involved in the regulation of hepatic glucose distal small bowel induces GLP-1 increases (up to metabolism by the nuclear receptor Farnesoid X Receptor threefold), which is secreted by L-cells from the gut and (FXR) pathways. The FXR is highly expressed in the liver improves beta cell function and insulin sensitivity (54). and intestine, but also in adipose tissue, the pancreas and The important role of GLP-1 has been demonstrated in the adrenal glands. BA can also improve the glucose profile studies using GLP-1 receptor antagonists that eliminate indirectly via FXR-mediated induction of the fibroblast beneficial glycemic effects after RYGB (55). Postprandial growth factor 19 (FGF19) in the intestine (67, 68, 69). levels of GLP-1 are observed to be enhanced after both SG A recent animal study conducted by Kohli et al. (70) has and RYGB in human and rodent models, suggesting that demonstrated the metabolic effect of diverting bile to the alterations in intestinal hormone secretion are of signi- distal gut. The investigators placed a catheter into the ficant importance with respect to the metabolic benefit of common bile duct of obese rats to drain bile to the distal these procedures (56, 57, 58). Changes in GLP-1 levels part of the jejunum. The results highlighted the role of BA were studied in T2DM obese patients (T2DM for !5 years) in glucose homeostasis control. Unfortunately, only a few before and 1 month after RYGB. Interestingly, oral human studies have addressed the role of BA in diabetes glucose-stimulated GLP-1 (AUC) and gastric inhibitory control after bariatric surgery (71). Patti et al. (71) peptide (GIP) peak levels increased significantly, performed a cross-sectional analysis of fasting and post- compared to controls (59). Despite this, some authors meal serum BA and metabolic variable composition in have suggested that GLP-1 is likely not involved in three groups of subjects; post-RYGB group (nZ9), non- diabetes improvement after bariatric surgery (60). RYGB group matched to preoperative BMI (nZ5), and non- Functional studies designed to assess the influence of RYGB group matched to current BMI (nZ10). Total serum GLP-1 signaling have obtained mixed results (57, 58, 61). BA concentrations were significantly higher in the RYGB

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group compared to the other two groups. Total BA were our institution evaluated diabetic nephropathy changes also inversely correlated with 2-h post-meal glucose and after bariatric surgery (81). We followed patients over a fasting triglycerides and positively correlated with adipo- 5-year period measuring urinary albumin excretion nectin and peak GLP-1 (follow-up study at 24–48 months). serially. Preoperatively, 37.8% of patients had microalbu- One target of FXR signaling is the gut bacterial flora minuria or macroalbuminuria. After a mean follow-up of (72). Recent findings suggest that intestinal bacteria have 5.5 years, the abnormal albuminuria resolved in 58.3% of an impact on host metabolism, obesity and diabetes (73). patients after surgery (81). Another non-randomized study It has been observed that gastrointestinal rearrangements of the effects of BPD vs medical treatment on diabetic after RYGB promote substantial changes on the gut complications (nZ110) studied long-term renal function microbiota (74). Studies in mice surrounding fecal after both treatments. Fifty patients completed the 10-year transplants from RYGB-treated animals have shown study. Renal function was preserved over 10 years in the substantial weight loss in comparison with mice BPD group and decreased in the medically treated group containing fecal transplants from sham-treated mice, (glomerular filtration rate C13.6% vs K45.7%) (80). thus suggesting that changes in gut bacteria after RYGB Furthermore, the STAMPEDE STUDY showed improve- can modulate body weight of the host organism (75). ment of albuminuria in both surgical groups. The urinary albumin-to-creatinine ratio (milligrams of albumin to grams of creatinine) decreased from a median of 9–6 in Cardiovascular risk the RYGB group (PZ0.08) and from 12 to 7 in the SG Bariatric surgery has been shown to resolve or improve group (P!0.001), as compared with the decrease from 6.5 cardiovascular risk factors such as diabetes, hypertension to 5.5 in the medical arm (PZ0.77) (46). and dyslipidemia (38, 41, 48, 76). For instance, Sugerman Weight loss surgery has also been shown to improve et al. (76) studied 521 hypertensive patients undergoing cardiac function and reverse remodeling of the heart up RYGB and reported hypertension resolution rates at 1 and to 3 years postoperatively (82). Surgery can improve all 5–7 years after surgery of 66 and 69%, respectively, with phases of obesity-related cardiomyopathy, and can superior outcomes in subjects achieving more EWL. improve left ventricular systolic function in patients Similar effects were reported in Buchwald’s meta-analysis, with severe heart failure who are awaiting heart trans- which demonstrated a hypertension resolution rate of plantation (83). However, long-term microvascular and 62% and improvement in 17% of patients (16). The macrovascular benefits after bariatric surgery will require retrospective cohort study by Adams et al. (77) also showed large multicenter clinical trials.

European Journal of Endocrinology sustained decreases in blood pressure during a 10-year period after surgery. However, the SOS study investigators Mortality suggest that hypertension seems to reappear in the context of weight regain, even with an overall weight The major goal of bariatric surgery is to decrease mortality. reduction (14). A meta-analysis including 44 022 participants from eight Weight loss surgery promotes substantial decreases in trials (mean follow-up of 7.5 years) showed reduced risk triglycerides levels as well as improvements in cholesterol of global mortality (ORZ0.55, CI 0.49–0.63) and cardio- profiles (16, 78). Zlabek et al. (78) showed a 41% reduction vascular mortality (ORZ0.58, CI 0.46–0.73) after bariatric in serum triglycerides 1 year after RYGB, an elevation in surgery compared with controls (no surgery) (84). Actually, HDL cholesterol by 23% and lowering of LDL cholesterol weight loss surgery can reduce mortality by 30% (85).In by 19%, with sustained beneficial effects on cholesterol the SOS trial, over a period of up to 10 years, mortality was profiles up to 2 years follow-up. A long-term follow-up significantly lower in the surgical group (5.0%) than in the study of morbidly obese patients with T2DM (nZ219) control group (6.3%), representing a hazard ratio (HR) of reported a 40% decrease in triglyceride levels and 20% 0.76 (95% CI 0.59–0.99, PZ0.004). It should be noted that increase in HDL-C levels (79). These improvements were while the SOS study was not sufficiently powered to maintained 2–4 years after surgery. establish specific causes of death, the most common were Very little is known about the effect of bariatric attributable to cardiovascular-related causes (68). A retro- surgery on reducing the vascular complications of spective cohort study by Adams et al. (77) compared long- T2DM. Observational studies have suggested that bariatric term mortality in patients who underwent RYGB (nZ7925) surgery may reduce long-term renal impairment associ- with obese control patients matched for age, sex and BMI ated with diabetes (41, 80). A recent study conducted by (nZ7925). During a mean follow-up of 7 years, all-cause

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Received 5 June 2015 Revised version received 15 August 2015 Accepted 3 September 2015 European Journal of Endocrinology

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